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Historical and contemporary influence of the Leeuwin Currenton the marine biota of the southwestern AustralianContinental Shelf and the Recherche Archipelago

G A Kendrick1, N A Goldberg1, E S Harvey1 & J McDonald1,2

1 School of Plant Biology,University of Western Australia,

35 Stirling Highway, Crawley, WA, 6009� [email protected]

2 Western Australian Fisheries & Marine Research Laboratories,39 Northside Drive, Hillarys, WA, 6025

Manuscript received February 2008; accepted January 2009

Abstract

The influence of the Leeuwin Current on the marine biota of the southern continental shelf ofWestern Australia is investigated by incorporating geological, oceanographic and evolutionarycontexts. The effect of this seasonal current was found to have had an influence for approximately40 million years as inferred from palaeontological evidence. The effect has been observed despitesignificant variation in the southward movement of the Leeuwin Current, sea level fluctuations,continental climate and the northward movement of the Australian continent. The marine floraand fauna of the Recherche Archipelago demonstrated the scale of the Leeuwin’s reach withmacroalgae, demersal fish, molluscs and other invertebrates having greater affinity with thesouthern temperate flora and fauna, with a small percentage of subtropical species transportedeastward on the Leeuwin Current. A more detailed comparison of benthic macroalgal assemblagesindicated significant differences between the Recherche, the southern temperate flora in SouthAustralia at Isles of St Francis and the southwestern flora at Hamelin Bay, near Cape Leeuwin.These macroalgal assemblages were characterized by multiple species differences among theregions but also very high local species turnover (alpha diversity) among locations within eachregion. The relatively warm water and low seasonal variability in sea temperatures associated withthe winter flow of the Leeuwin Current may have played a major role in the persistence of warmwater species on the southern coast and the high species turnover we have observed over 18degrees of longitude. The Leeuwin Current has played a major but not an exclusive role in theevolution and persistence of this flora as well as the species richness and endemism of othermarine organisms along the southern coast of Western Australia.

Keywords: Leeuwin Current, Recherche Archipelago, southern Western Australia, evolution,macroalgae, diversity, alpha diversity

Journal of the Royal Society of Western Australia, 92: 211–219, 2009

© Royal Society of Western Australia 2009

Introduction

This paper characterizes the effect of the LeeuwinCurrent on biota along the southern shores of WesternAustralia and more specifically the effect of the Currenton the Recherche Archipelago. We summarize a body ofliterature that includes the effect of geological andcontemporary processes on the biology, distribution andbehavior of marine organisms found along the southcoast and then more specifically for RechercheArchipelago. As a case study, the relationship thatassemblages of marine macroalgae in the RechercheArchipelago have with the flora of southwest andsouthern Australia is then addressed. The paper thenconcludes with hypotheses about the potential causalmechanisms for the biogeographic relationships.

The Continental Shelf of southern Western Australia

The continental shelf off southwestern Australiaextends from Israelite Bay at the western edge of theGreat Australian Bight to Cape Leeuwin, covers an areaof nearly 65,000 km2 and is characterised by a 30–65 km-wide continental shelf that slopes gently to a depth of100 m. It contrasts with the flat and gently sloping shelfof the main Great Australian Bight region east of theRecherche Archipelago (James et al. 1994). Furtheroffshore, the seafloor drops away quickly after the shelfbreak at between 100 m and 140 m depth. In the east, theshelf is up to 65 km wide and punctuated by the graniticislands of the Recherche Archipelago (Conolly & von derBorch 1967). These islands are scattered across the entirewidth of the shelf and extend for more than 160 km alongthe coast. Sediments around the Recherche Archipelagoare characterised by marine biogenic carbonates offshoreand silica rich sediments onshore, that are eroded fromthe granites and gneisses of the archaean shield thatcovers a large proportion of southwestern Australia(Ryan et al. 2007). The shelf varies between 30 km and

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Journal of the Royal Society of Western Australia, 92(2), June 2009

65 km in width to the west of the archipelago, but mostislands in the western portions of the shelf occur within8 km of the mainland (Conolly & von der Borch 1967).

Numerous canyons incise the continental slope to thewest of the Great Australian Bight. These include thePasley and Esperance canyons offshore from theRecherche Archipelago, and the Albany Canyon Group(>30 canyons), which dissect the continental slope atregular intervals between Hood Point and PointD’Entrecasteaux (von der Borch 1968). Recent sonarsurveys in the Albany Canyon Group have shown thatsome individual canyons are up to 2000 m deep and90 km long, and extend uninterrupted between the shelf-break and the abyssal plain (Exon et al. 2005).

The southern continental shelf is heavily influencedby large, deeply abrading ocean swells that erode theshelf in depths up to 100m, with greatest abrasion of thebottom in the mid shelf region between 50 and 90 mdepths (James et al. 1994). Contemporary sediments donot accumulate and the sediments that do accumulateare mixtures of reworked Pleistocene and recentsediments (Conolly & von der Borch 1967). An exampleof the scale of the effect of ocean swells on the southwestern continental shelf can be gleaned from Hemer(2006) who, in determining combined shear stress acrossthe whole of the Australian continental shelf, found thatin 48 metres depth off Cape Naturaliste, WesternAustralia, mean (maximum) wave periods recorded were7.5 sec (15.7 sec), significant wave heights were 2.2 m(11.5 m) giving a combined benthic shear stress of 1.20Nm-2 (85.9 Nm-2), making it one of the highest energysites in temperate Australia.

Palaeo-oceanography and the Leeuwin Current

The effect of the Leeuwin current or earlier proto –Leeuwin currents on water temperature and mixing oftropical species along the temperate south coast ofWestern Australia has been effective since the middle tolate Eocene (35–42 Mya) (McGowran et al. 1997). Pelagicand benthic Foraminifera has been used to build achronological palaeo-history of warm water transportsouthward along the west and south western coasts ofAustralia (Cann & Clarke 1993; Wells & Wells 1994; McGowran et al. 1997; Li et al. 1999) There have beendocumented geological periods when the current seemsto have been inactive (Early to Middle Oligocene, EarlyPliocene) and reactivated (Early to Middle Miocene). TheLeeuwin current strengthened in the middle to latePleistocene and enhanced the southward transport ofmore tropical species (Anadara trapezia arcoid bivalve andAcropora corals) in southwest Australia and the inshoresurface water temperatures during the last interglacial(122 –120 kyr BP) were > 2°C than they are today(Kendrick et al. 1991; McGowran et al 1997; Murray-Wallace et al. 2001). More recently during the lateQuaternary, water north of 18°S varied little intemperature despite large extremes in climate, whereasfurther south there was significant changes to surfacewater temperatures, suggesting southward influence ofthe Leeuwin Current was disrupted during both glacialand interglacial extremes (Wells & Wells 1994).

There is a strong longitudinal temperature gradientand faunal pattern along the southern coastline of

Western Australia generated by the Leeuwin Current.Larger benthic foraminifera show a west to east gradientin occurrence along the southern coast of WesternAustralia, with the genera Heterostegina, Amphistegina,Amphisorus and Planorbulinella common in sediments atCape Leeuwin (115°S), Amphistegina, Amphisorus andPlanorbulinella at Albany (117°S), and only Amphisorus atEsperance (122°E) (Li et al. 1999). At Esperance, thepresence of tropical foraminifera, especially the benthicAmphisorus (Marginopora) taxon, both as living and inreworked sediments (120,000 yr BP) infer that thesouthward movement of the historical and contemporaryLeeuwin Current has heavily influenced the benthicassemblages in this region at least since the lastinterglacial (Cann & Clarke 1993; Li et al. 1999).

As the Leeuwin Current seasonally flows duringwinter months and is episodic in strength of flow andinfluence on the south coast, it is quite amazing that ithas such long geological time scale influences on benthicorganisms as demonstrated for the arcoid bivalves(Kendrick et al. 1991) and benthic and pelagicforaminifera (Li et al. 1999).

The effects of sea level fluctuations and wave abrasionover the same geological period do not appear to weakenthe overriding influence of the west to east gradient inthe strength of the Leeuwin Current. Interestingly, Li etal. (1999) found the benthic foraminiferal assemblagesduring the late interglacial period were representative oflagoonal environments whereas recent assemblages weremore representative of shallow open shelf environments.

The Contemporary Leeuwin Current on the SouthCoast of Western Australia

The Leeuwin Current moves eastward over thewestern shelf (Albany to Bremer Bay) moving offshorenear the shelf break further eastward (RechercheArchipelago) and is strongest during winter. It warmssea-temperatures, and bathes the coastline with lownutrient waters. Light is generally less limiting to benthicand planktonic primary producers on the innercontinental shelf and water column attenuationcoefficients are very low, as water column turbidity fromphytoplankton blooms and from river discharges aresmall (k

d = 0.08: Carruthers et al. 2007). The surface

waters of the southwestern Australian shelf, waters ofthe Leeuwin Current and surface waters offshore arevery low in nitrogen (less than 0.5 μmol) year round andprimary productivity is nitrogen limited (Lourey et al.2006).

Characteristics of Flora and Fauna on the south coast

The southwestern corner of Australia is a region ofhigh species diversity and endemism for many marineorganisms; for example, marine macroalgae (Womersley1990; Phillips 2001), invertebrate taxa such as molluscsand echinoderms and decapod crustaceans(Wells et al.2005; O’Hara & Poore 2000), and nearshore (Hutchins1994) and continental slope demersal fish (Williams et al.2001). High species richness in the region is attributed tothe lack of mass extinction events associated withunfavorable environmental conditions – such asglaciation – over the recent geological past, and themoderating influence of the Leeuwin Current since the

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Eocene (McGowran et al. 1997). The high endemism ofthe region is a product of long isolation of the marineflora and fauna as Australia has been separated fromother land masses for the past 80 million years (Veevers1991; Phillips 2001).

Effects of Leeuwin Current on Demersal and MigratoryFish

The Leeuwin Current is regarded as the dispersalmechanism responsible for transporting subtropical andtropic fish species southwards along the west coast(Hutchins & Pearce 1994) and eastwards along the southcoast of Western Australia. The south coast of WesternAustralia is dominated by temperate demersal fishes thatare found across the whole southern shores of Australia,although there are increasing numbers of sub tropicalspecies from Israelite Bay to Cape Naturaliste (Hutchins2001). Only 56% of demersal fish species are sharedbetween the south coast, from Israelite Bay to CapeNaturaliste, and the lower west coast, Perth to PortDenison, and only 29 % with the central west coast, fromHoutmans Abrolhos to Kalbarri. (Hutchins 2001). Thisinfluence is not as strong in surf zone fish assemblages.There is a decrease in total number of surf zone fishspecies from the west coast (20–66 species) to the southcoast (11–16 species), and also a notable absence oftropical species in surf zone assemblages from the southcoast (Ayvazian & Hyndes 1995).. The influence of theLeeuwin Current is also evident on recruitment andrecruitment limitation. For example in pilchards(Sardinops sagax) along the south coast (Fletcher et al.1994) there was a strong eastward transport of pilchardeggs from Albany over 150 km distances within daysduring winter when the Leeuwin Current was at itsstrongest but not during summer, resulting ingeographical discontinuities in the early life histories ofsome populations of pilchards. This suggests that theLeeuwin Current influences fine spatial scale populationstructure in this highly mobile species. Interestingly,other highly mobile species are less influenced by theLeeuwin flow. The Australian herring (Arripis georgiana)is highly migratory and can be treated as a single stockfrom Victoria to southern Western Australia (Ayvazian etal. 2004).

Effect of the Leeuwin Current on Zooplankton

Both chaetognaths and siphonophores were betterrepresented and more speciose during winter thansummer (Gaughan & Fletcher 1997). Numbers of speciesdecreased along 11 cross-shelf transects between Albanyand Esperance in winter but not summer and thisgradient reflected the decline in numbers of tropicalspecies entrained in the Leeuwin Current during winter.The species of siphonophores and chaetognaths observedwere all characteristic of warm waters and no coldtemperate species were found.

Effect of the Leeuwin Current on Echinoderms andDecapod crustaceans

O’Hara & Poore (2000) analysed the distributions of739 species of temperate Australian echinoderms anddecapod crustaceans and noted that the western peak inspecies diversity at Perth, Western Australia, was 2degrees further south than the eastern peak in species

diversity at Sydney, New South Wales. Theirinterpretation of the geographical peaks in speciesrichness should be taken with caution as it is confoundedby sampling intensity and the proximity of Perth andSydney to State and commonwealth Museum andresearch groups specializing in invertebrates. There weremany endemic subtropical and tropical speciescharacteristic of the lower west coast and their moresouthern distribution was due to the influence of theLeeuwin Current in transporting subtropical and tropicalspecies southwards. The south coast of Western Australiafrom Albany to Eucla varies by only 2 degrees latitudeand has a few degrees change between summer andwinter water temperatures. O’Hara & Poore (2000) foundrelatively high species turnover, or replacement, acrossthis region and inferred that the higher wintertemperatures (Leeuwin Current) and small differencesbetween summer and winter temperatures have allowedsubtropical species to persist further east than may beexpected. This results in a longitudinal turnover frommore subtropical species to the west to more temperatespecies to the east but with little change in speciesrichness.

Effect of the Leeuwin Current on Macroalgae

Wernberg et al. (2003) combined quantitative surveysof macroalgal diversity on limestone reefs from Marmion,north of Perth, Hamelin Bay and Hopetoun andconcluded that there was a cline in overlapping speciesdistributions from the west coast to the south coast.Wernberg et al. (2003) inferred that this cline indicatedmixing of species from north to south, presumablythrough transport of propagules in the Leeuwin Current.They also found a shift in dominant canopy algae fromthe eurythermal Ecklonia radiata kelp forests common onthe west coast to E. radiata combined with more southerntemperate Scytothalia doryocarpa and Cystophora in thecentral south coast.

Influence of the contemporary Leeuwin Current on theRecherche Archipelago

The Recherche Archipelago is a group of 108 islandsand many small reefs between 122°E and 124°Elongitude. They are predominantly inshore on the shelfand are often not influenced by the main body of theLeeuwin Current that is situated on the outer continentalshelf and slope at these longitudes. Interestingly, theLeeuwin current flows out to sea from the shelf break tothe south of the eastern Recherche Archipelago, with anonshore movement of nutrient enriched sub-Antarcticwaters (Cresswell & Griffin 2004). The effect of thesecolder nutrient-rich sub-Antarctic waters on thecontinental shelf near the Recherche Archipelago isunknown. Cresswell & Griffin (2004) postulate that thissouthward movement of the Leeuwin Current may bedue to the 30o change in shelf orientation or the outflowof warmer waters from the Great Australian Bight or acombination of both. This offshore movement of theLeeuwin Current generates the strong anticyclonic eddiesthat develop south of the shelf break and arecharacteristic of waters south of the southern WesternAustralian continental shelf. The Recherche Archipelagois only seasonally bathed in Leeuwin Current waters andwater temperatures are generally colder than offshore

Kendrick et al.: Historical and contemporary influence of the Leeuwin Current

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waters, and inshore waters to the west except for themonths October and November (Figure 2 in Cresswell &Griffin 2004). Thus the overall strength of the LeeuwinCurrent may heavily affect the year to year influence onthe biota of the Recherche Archipelago.

Floral and Faunal characteristics of the RechercheArchipelago

We first summarise the contemporary distribution ofthe predominant benthic biota, and demersal fish in theRecherche Archipelago. Then, using the macroalgae asan example, we investigate what makes this regioninteresting and how it is related to the temperate flora tothe east and the subtropical and tropical flora associatedwith the west coast of Western Australia and theLeeuwin Current. We describe the importance ofconsistent ocean climate over millennia and its influenceon the diversity and endemism of the macroalgal floraand incorporate both contemporary ecology andhistorical biogeography in the description of the effectsof the Leeuwin Current on the marine benthos in thisregion.

Benthic Macroalgae of Recherche

Subtidal macroalgal assemblages of the RechercheArchipelago were more similar to macroalgalassemblages in South Australia and Victoria (Collings &Cheshire 1998; O’Hara 2001) than to thosepreviouslydescribed from the west coast and thesouthwestern region of Western Australia (Wernberg etal. 2003). Two hundred and forty two species have beenrecorded in the Recherche Archipelago, with 148 speciesof Rhodophyta, 65 species of Phaeophyceae, and 29species of Chlorophyta (Goldberg & Kendrick 2005)(Table 1). Range extensions were recorded for 37 species,28 were westward extensions from the temperatesouthern coast of Australia and 9 were eastern extensionsfrom southern and western shores of Western Australiawest of the Archipelago (Goldberg & Kendrick 2005).This demonstrates the temperate nature of algalassemblages in the Recherche Archipelago and also ourpoor knowledge of the marine flora along southernWestern Australia.

Marine Fauna of the Recherche Archipelago

Hutchins (2005) found the nearshore demersal fishfauna of the Recherche Archipelago totalled 263 species,with 68 species found only in Western Australia (Table

1). A barrier to eastward species dispersal was postulatedto exist at the western side of the Great Australian Bight.Wells et al. (2005) identified 347 species of molluscs fromthe Recherche Archipelago, 275 were temperate southernAustralian and 56 were Western Australian indistribution (Table 1). McDonald & Marsh (2005) describe12 seastars from the Recherche Archipelago, all but onewith a temperate southern distribution (Table 1).Similarly, of the 6 ascidians identified from Recherche,all had temperate southern distributions (McDonald2005). Seventy seven hydroids were recently describedfrom the Recherche Archipelago, 6 new species onlyknown from the Archipelago, 58 with southerntemperate distributions and only 5 restricted to WesternAustralia (Watson 2005). Pycnogonids have more westcoast species (6) than southern temperate (5) and 1 newspecies only known from the Recherche Archipelago(Bamber 2005), although this trend has more to do withthe geographical sampling done by the expert than therealised distributions of pycnogonids.

In summary, the marine flora and fauna of theRecherche Archipelago are predominantly temperatesouthern Australian in affinity. There are few species thathave west coast distributions, supporting the model thatthe Recherche Archipelago is less influenced by theLeeuwin Current. Interestingly, the Leeuwin Currentmay still act as a barrier to western transport of southernAustralian temperate species. This requires furtherinvestigation.

Relationship of the macroalgal flora of RechercheArchipelago with Hamelin Bay, WA and the Isles of StFrancis, South Australia

Our objective was to test if the marine flora of theRecherche Archipelago (RA) was similar to that ofrepresentative floras of the south west flora documentedat Hamelin Bay, Western Australia or the southernAustralian flora east of the Great Australian Bight, fromthe Isles of St Francis, near Ceduna, South Australia.Rather than a full biogeographical analysis like that ofO’Hara & Poore (2000), we have focused in on specificlocalities that are representative of the south westernregion (Wernberg et al. 2003; Kendrick et al. 2004; Tooheyet al. 2007) and the southern region, east of the GreatAustralian Bight (Womersley & Baldock 2003). Thisdecision was made because floristic sampling along thesouthern shores of Western Australia have been limitedto a few field surveys and the taxonomic data from

Table 1

Description of the species richness and relationships of selected groups of the flora and fauna of the Recherche Archipelago withwestern and southern temperate Australia.

Taxon Recherche Only known Southern Western AuthorSpecies from Temperate AustraliaRichness Recherche Australia

Seaweeds 234 0 186 17 Goldberg & Kendrick 2005Fish 263 0 189 68 Hutchins 2005Molluscs 347 0 275 56 Wells et al. 2005Sea stars 12 0 11 1 McDonald & Marsh 2005Ascidians 6 0 6 0 McDonald 2005Hydroids 77 6 58 5 Watson 2005Pycnogonids 15 1 5 6 Bamber 2005

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opportunistic collections, many from the drift on beaches(see Womersley 1984, 1987, 1994, 1996, 1998, 2003)

Species presence information for macroalgae for thesouth west flora were taken from collections made in2006 from 18 locations in Hamelin Bay (n = 54 x 0.25 m2

quadrats) (Figure 1) . This is part of a 6 year temporalstudy described in Kendrick et al. (2004) and Toohey et al.(2007). The Recherche Archipelago flora was compiledfrom surveys of 11 islands (Figure 1) conducted inOctober of 2003 and 2004 (n = 372 x 0.25 m2 quadrats)(Goldberg & Kendrick 2004; Goldberg et al. 2006). Similarspecies data was taken from a survey of the Isles of StFrancis from 12 locations (Figure 1) by Womersley &Baldock (2003). These data differ from the other locationsas they are not quadrat samples but actual species listsfrom each location.

Multivariate tools were used to illustrate differencesamong floras in the southern coast of Australia. Non-metric multidimensional scaling (MDS) was used on aBray-Curtis similarity matrix of species presence/absencedata, equivalent to a Sorenson coefficient, from all threeregions (PRIMER Vers. 6). A one-way permanova testedthe significance of differences in macroalgal assemblagesamong Isles of St Francis, Recherche and Hamelin Bay(Anderson 2001). A similarity percentages analysis wasconducted to assess the average similarity within versusamong regions.

We found all three regions separated clearly in twodimensions on the MDS plot (Figure 2). They did not

form a cline as demonstrated by Wernberg et al. (2003)for the south western algal flora, but were distinctgroupings. Both Hamelin Bay (SW) and the RechercheArchipelago (RECH) formed tight clusters whereas thelocations from the Isles of St Francis (FRANCIS) weremore dispersed. This difference was possibly driven bythe difference in sampling intensity between regions;Isles of St Francis were qualitative species lists madefrom collections at locations whereas both Recherche andHamelin Bay were quantitative samples taken usingquadrats. The permanova on species presence/absence(Table 2) and pairwise tests between regions (Table 3)demonstrated that macroalgal assemblages in all 3regions were highly significantly different.

The average similarity accounted for by among andwithin regions demonstrates some overlap in speciespresence/absence among regions (Table 4). Themacroalgal assemblage in Hamelin Bay (SW) sharedalmost 25% with the Recherche Archipelago (RECH) butonly 14% with the Isles of St Francis (FRANCIS). TheRecherche Archipelago shared approximately 21% withthe Isles of St Francis. Clearly, these flora are not thatsimilar among regions. What is driving this difference?The shared similarity among locations with regions alsois small (diagonals in Table 4). Locations within regionsshared less than 50% of species for both Hamelin Bayand the Recherche Archipelago. From the species listsfrom the Isles of St Francis it was less than 22%. Clearlythe macroalgal flora within each region shows high levels

Figure 1. A. Map of Australia showing locations mentioned in the text and the CONCOM marine biogeographic regions LWC = LowerWest Coast, SWC = South West Coast, GAB = Great Australian Bight, SGC = South Gulfs Coast, BS = Bass Strait, TC = TasmanianCoast, LEC = Lower East Coast, and CEC = Central East Coast and the Recherche Archipelago (RA), with inset maps of the three studylocations: Hamelin Bay, Recherche Archipelago and Isles of St Francis.


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of species turnover among locations. The speciesresponsible for the differences among and within regionswere many with no species contributing more than 1.6 %to the overall percentage of dissimilarity among theregions.

Discussion

The macroalgal flora and fauna of the RechercheArchipelago is more similar to the temperate flora foundalong southern shores of Australia. Separation of thesouth coast of Australia from Antarctica beganapproximately 90 million years ago and ended 30 millionyears ago with oceanic water flowing between the twocontinents (Poore 1994). During this period of separationbetween Australia and Antarctica, the macroalgal flora inthe shared waters between the two continents waspresumably Tethyan in origin (Phillips 2001). Clayton(1994) speculated that prior to formation of sheet-ice,Antarctic macroalgal species richness was similar to thatof temperate southern Australia, particularly for speciesin the Phaeophycean order Fucales (e.g., Cystophora andSargassum species). Coastal sea temperatures haveremained temperate as the continent moved with thenortherly drift of the Australian plate, with a warm-water influx from the Leeuwin Current along the westcoast (Phillips 2001). This has resulted in southward andeastward transport of subtropical species from centraland northern Western Australia. These subtropicalspecies are a small percentage of the predominantlytemperate flora and fauna found in the RechercheArchipelago.

Species replacement (turnover) of the marinemacroalgae from east to west along the southern shoresof southwestern Australia is great, although, species

Table 3

Pairwise comparisons between Hamelin Bay (SW), theRecherche Archipelago (RECH) and the Isles of St Francis(FRANCIS).

Groups t P(perm) perms

SW, RECH 3.3896 0.0001 9872

SW, FRANCIS 2.2909 0.0001 7661

RECH, FRANCIS 3.0584 0.0001 9912

Table 4

A matrix of the average similarity of macroalgal assemblageswithin and among regions along the south western and centralcoast of Australia. SW = Hamelin Bay, RECH = RechercheArchipelago, FRANCIS = Isles of St Francis)

SW RECH FRANCIS

SW 48.71

RECH 24.96 48.43

FRANCIS 14.40 20.61 21.88

Table 2

One- Factor Permanova comparing species presence macroalgalassemblage data from the 3 regions (Hamelin Bay, RechercheArchipelago and the Isles of St Francis) along the south westernand central coast of Australia.

Source df MS Pseudo-F P(perm)

Regions 2 16243 8.8009 0.0001

Residual 41 1845.6

Total 43

Figure 2. Non-metric two-dimensional multidimensional scaling plot (MDS) depicting the relatedness of subtidal macroalgalassemblages (using species presence) among SW (Hamelin Bay), RECH (Recherche Archipelago) and FRANCIS (Isles of St Francis).

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richness from Isles of St Francis to Hamelin Bay issimilar. The majority of the replacement is a switch fromsouthern temperate species to endemic south westernspecies to more prevalence of subtropical speciessuggesting an increase in influence of the LeeuwinCurrent from east to west. For example, subtropical andtropical species from central and northern WesternAustralia are a small percentage of the flora of theRecherche Archipelago. Echinoderms and decapodcrustaceans show a similar east to west speciesreplacement with little change in species richness(O’Hara & Poore 2000).

How can we account for the pattern in speciesreplacement at local and regional scales across southernWestern Australia? The contemporary Leeuwin Currentaids in dispersal of tropical and subtropical species to thesouthern coast of Western Australia, depresses upwellingresulting in high ambient light conditions at depth andreduces the seasonal variation in nearshore seawatertemperatures. Yet diversity of marine organisms asdemonstrated by benthic algae in this study, andechinoderms and decapod crustaceans by O’Hara &Poore (2000) is not solely driven by contemporaryprocesses alone. Historically the influence of warmerwaters further south in temperate Australia has resultedin high diversity, endemism and local speciesreplacement.

The long term effect of the northward driftingAustralian continent and the moderating effect of thewarm Leeuwin Current have resulted in a diverse andhighly endemic marine macroalgal flora (Phillips 2001).Isolation can explain the endemism but what historicallyhas produced and maintained the diversity? High localspecies replacement is a signature of the benthicmacroalgae of this region (Kendrick et al. 1999, 2004;Goldberg & Kendrick 2004; Toohey et al. 2007). Wernberget al. (2003) found 33% of nested variation in speciesrichness was accounted for by local species turnover.Similarly, Goldberg & Kendrick (2004) foundapproximately 60% of all macroalgal species found in adetailed survey of 6 islands in the western RechercheArchipelago were rare, occurring as less than 5 gm wetweight across 216 quadrats where the average algalbiomass from the quadrats was 1kg or more. Sixtypercent of 220 macroalgal species accounted for this localscale species replacement. Kendrick et al. (1999) reportedthat similar high local species replacement, or turnover,was not accounted for by differences between reefs andexposure to ocean swells at Marmion, on the west coastof Western Australia.

What drives local species replacement? This is notassociated with any broad scale oceanographic gradientsbut to the successful colonisation and maintenance ofsmall local populations. What aspect of this marineenvironment is so unique that it has historicallypromoted and in contemporary time scales maintainedsuch high alpha, or local diversity? Ecological theoryabout species coexistence suggests a series of interrelatedprocesses support the high species turnover we haveobserved. Firstly, competitive networks can be decoupledand the major factor usually invoked is the frequencyand extent of biological and physical disturbances.Competitive networks may also not be established if theassemblages are not density-dependent.

Macroalgal species can produce up to millions ofreproductive propagules per thallus (Kendrick & Walker2005), although dispersal is thought to be limiting aspropagules have a small planktonic lifespan. Successfuldispersal and recruitment into a density-independentadult population can result in decoupling of competitionand the co-existence of many species. The stochasticnature of disturbance and recruitment temporally andspatially can also result in patchy spatial distribution ofspecies, especially when associated with highlycompetitive species like the kelp Ecklonia radiata, commonon temperate coasts of Western Australia. The frequencyand size of the gap creating disturbance and time ofrecolonization of gaps in kelp forests determines thebiomass and species richness of macroalgae in theassemblage (Toohey et al. 2007). Once competition fromthe kelp is reduced the number of species colonising thereef increases dramatically although the biomass of theassemblage is small. As the kelp recolonises the gapsspecies richness declines and overall biomass increases(Toohey et al. 2007).

The realized niche concept is poorly identified formarine benthic flora and fauna although much of theobserved small scale species replacement may be drivenby very fine scale differences in the reef that affect whatspecies colonise it (Toohey & Kendrick 2008). Recentwork on the effect of reef topography on assemblagestructure and diversity of macroalgae has demonstratedthat competitive interactions on complex reefs can bereduced and diversity increased through increasingniches and through niche overlap for foliose algae.Rugose, topographically complex reefs affect the strengthand direction of competition by Ecklonia radiata (Toohey& Kendrick 2008). This spatial complexity enhances thenumber of species associated with kelp forests, whereasin a topographically poor planar reef the negative effectof kelps on the colonisation and persistence of othermacroalgae is more evident (Kendrick et al. 1999; Tooheyet al. 2007).

Other canopy forming macroalgae do not showsimilar competitive dominance. Goldberg (2007)demonstrated that patterns in algal colonisation undercanopies of Cystophora and Sargassum in the RechercheArchipelago were maintained by processes other thancompetition with the canopy species. Clearly the effect ofcanopy can be uncoupled either by the release fromcompetition via disturbance, provision of niches throughreef rugosity or through mechanisms other than directcompetition by canopy species.

Historically, the species rich benthic flora and faunahave persisted on the southern coast of Western Australiabecause it evolved in geographical isolation, has notsuffered major extinction events, glaciation in recentgeological past (Holocene) nor major shifts in currentssince the Eocene (McGowran et al. 1997). Valdovinos et al.(2003) demonstrated that regional context and historydefines the distribution and abundance of southerntemperate Pacific molluscs. Their explanation for highermollusc biodiversity in cold temperate waters thansubtropical and tropical waters was the combined effectsof increased continental shelf surface area, refugia duringglaciation events and the divergence of species throughgeographical isolation associated with historical andpresent currents. Similarly, the lagoonal environments


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reported from benthic foraminifera assemblages duringthe late interglacial period (Li et al. 1999) suggest thatbenign environments for marine organisms have existedat least into the recent geological past. We report algalspecies replacement but no real change in speciesrichness from east to west along the south-westernAustralian continental shelf. Hamelin Bay in thesouthwestern tip of Western Australia has an assemblageof algae distinct from that of the Recherche Archipelago,and the Isles of St Francis at the eastern extent of theGreat Australian Bight. This rate of species replacement,or turnover, over 18 degrees of longitude in southernAustralia has already been reported for decapodcrustaceans (O’Hara & Poore 2002). Their explanationhinges on both global isolation and regional connectanceof species across the whole southern temperatecontinental shelf over the last 80 million years, combinedwith warming of waters as Australia has movednorthward resulting in isolation and extinction of somespecies and southward moving warm water currentsfrom the tropics on both the western and eastern coastsof Australia bringing warm temperate, subtropical andtropical species into more temperate latitudes. Localspecies replacement (alpha diversity) is extremely highin seaweed assemblages and we list what we believe areimportant local processes that have led to this situation.Similarly, Huston (1999) defines local processes (andtheir interaction with regional processes) in the evolutionof diverse groups of organisms. He emphasizes the needfor greater understanding of species niche concept andscaling studies of patterns in distribution and abundancesuch that they are sampled across scales that are relevantto the processes that have defined the survival andevolution of organisms. In benthic algae, local speciesturnover appears to be associated with release fromcompetitive hierarchies, physical disturbance, high levelsof recruitment and broad niche requirements.

In temperate Western Australia, historical andcontemporary processes have resulted in a globallyimportant, speciose endemic hotspot for marine flora andfauna. The Leeuwin Current has played a major but notan exclusive role in the evolution and persistence of thisflora and fauna along the southern coast of WesternAustralia.

Acknowledgements: For the Recherche Archipelago data we acknowledgethe valuable grant from the Fisheries Research and DevelopmentCorporation (FRDC 2001/060) and the Western Australian StrategicResearch Fund for the Marine Environment. For the Hamelin Bay data weacknowledge funding from the Foundation for Research, Science andTechnology, New Zealand who provided a Postdoctoral Fellowship to E.H. and a small Australian Research Council grant to G. K.

References

Anderson M J 2001 A new nonparametric multivariate analysisof variance. Austral Ecology 26: 32–46.

Ayvazian S G, Bastow T P, Edmonds J S, How J & Nowara G B2004 Stock structure of Australian herring (Arripis georgiana)in southwestern Australia. Fisheries Research 67: 39–53.

Ayvazian S G & Hyndes G A 1995 Surfzone fish assemblages inthe southwestern Australia: do adjacent nearshore habitatsand the warm Leeuwin Current influence the characteristicsof the fish fauna? Marine Biology 122: 527–536.

Bamber R N 2005 The pycnogonids of Esperance, WesternAustralia. In: The Marine Flora and Fauna of Esperance,

Western Australia (eds F E Wells, D I Walker & G AKendrick). Western Australian Museum, pp 325–341.

Brearley A 2005 Ernest Hodgkin’s Swanland: estuaries andcoastal lagoons of southwestern Australia. UWA Press, Perth.

Cann J H & Clarke J D A 1993 The significance of Marginoporavertebralis (Foraminifera) in surficial sediments at Esperance,Western Australia and in late interglacial sediments innorthern Spencer Gulf, South Australia. Marine Geology 111:171–187.

Carruthers T J B, Dennison W C, Kendrick G A, Waycott M,Walker D I & Cambridge M L 2007 Seagrasses of southwestAustralia: A conceptual synthesis of the world’s most diverseand extensive seagrass meadows. Journal of ExperimentalMarine Biology and Ecology 350: 21–45.

Clayton M N 1994 Evolution of the Antarctic marine benthicalgal flora. Journal of Phycology 30: 897–904.

Collings G J & Cheshire A C 1998 Composition of subtidalmacroalgal communities of the lower gulf waters of SouthAustralia, with reference to water movement andgeographical separation. Australian Journal of Botany 46:657–669.

Conolly J R & von der Borch CC 1967 Sedimentation andPhysiography of the sea floor south of Australia.Sedimentary Geology 1: 181–220.

Cresswell G R & Griffin D A 2004 The Leeuwin Current, eddiesand subAntarctic waters off southwestern Australia. Marine& Freshwater Research 55: 267–276.

Exon N F, Hill P J & Post A 2005 Nature and origin of thesubmarine Albany Canyons off southwest Australia.Australian Journal of Earth Sciences 52: 101–115.

Fletcher W J, Tregonning R J & Sant G J 1994 Interseasonalvariation in the transport of pilchard eggs and larvae offsouthern Western Australia. Marine Ecology Progress Series111: 209–224.

Gaughan D J & Fletcher W J 1997 Effects of the Leeuwin currenton the distribution of carnivorous macrozooplankton in theshelf waters off southern Western Australia. Estuarine,Coastal and Shelf Sciences 45: 89–97.

Goldberg N A 2007 Colonization of subtidal macroalgae in afucalean dominated algal assemblage, southwesternAustralia. Hydrobiologia 575: 423–432.

Goldberg N A & Kendrick G A 2004 Effects of island groups,depth, and exposure to ocean waves on subtidal macroalgalassemblages in the Recherche Archipelago, WesternAustralia. Journal of Phycology 40: 631–641.

Goldberg N A & Kendrick G A 2005 A catalogue of the marinemacroalgae found in the western islands of the RechercheArchipelago (Western Australia, Australia) with notes ontheir distribution in relation to island location, depth, andexposure to wave energy. In: The Marine Flora and Fauna ofEsperance, Western Australia (eds F E Wells D I Walker & GA Kendrick). Western Australian Museum, pp 25–89.

Goldberg N A, Kendrick G A & Walker D I 2006 Do surrogatesdescribe patterns in marine macroalgal diversity in theRecherche Archipelago, temperate Australia? AquaticConservation: Marine & Freshwater Ecosystems 16: 313–327.

Hemer M A 2006 The magnitude and frequency of combinedflow bed shear stress as a measure of exposure on theAustralian continental shelf. Continental Shelf Research 26:1258–1280.

Huston M A 1999 Local processes and regional patterns:appropriate scales for understanding variation in thediversity of plants and animals. Oikos 86: 393401.

Hutchins J B 1994 A survey of the nearshore reef fish fauna ofWestern Australia’s west and south coasts the LeeuwinProvince. Records of the Western Australian MuseumSupplement 46: 1–66.

Hutchins J B 2001 Biodiversity of Shallow reef fish assemblagesin Western Australia using a rapid censusing technique.Records of the Western Australian Museum 20: 247–270.

219

Hutchins J B 2005 Checklist of marine fishes of the RechercheArchipelago and adjacent mainland waters. In: The MarineFlora and Fauna of Esperance, Western Australia (eds F EWells D I Walker & G A Kendrick). Western AustralianMuseum, pp 425–449.

Hutchins J B & Pearce AF 1994 Influence of the Leeuwin Currenton tropical fish recruitment at Rottnest Island, WesternAustralia. Bulletin of Marine Science 54: 245–255.

James N P, Boreen T D, Bone Y & Feary D A 1994 Holocenecarbonate sedimentation in the west Eucla Shelf, GreatAustralia Bight: a shaved shelf. Sedimentary Geology 90:161–177.

James N P, Bone Y, Collins L B & Kyser T K 2001 Surficialsediments of the Great Australian Bight: facies dynamics andoceanography on a vast coolwater carbonate shelf. Journal ofSedimentary Research 71: 549–567.

Kendrick GA & Walker D I 1995 Dispersal of propagules ofSargassum spp. (Sargassaceae, Phaeophyta): observations oflocal patterns of dispersal and possible consequences forrecruitment and population structure. Journal ofExperimental Marine Biology and Ecology 192: 273–288.

Kendrick G A, Lavery P A & Phillips J C 1999 Influence ofEcklonia radiata kelp canopy on structure of macroalgalassemblages in Marmion Lagoon, Western Australia.Hydrobiologia 398/399: 275–283.

Kendrick G A, Harvey E S, Wernberg T, Harman N & GoldbergN 2004 The role of disturbance in maintaining diversity ofbenthic macroalgal assemblages in southwestern Australia.The Japanese Journal of Phycology 51: 59.

Kendrick G W, Wyroll K H & Szabo B J 1991 PliocenePleistocenecoastal events and history along the western margin ofAustralia. Quarternary Science Reviews 10: 419–439.

Li Q, James N P, Bone Y & McGowran B 1999Paleoceanographic significance of recent foraminiferalbiofacies on the southern shelf of Western Australia: apreliminary study. Palaeogeography, Palaeoclimatology,Palaeoecology 147: 101–120.

Lourey M J, Dunn J R & Waring J 2006 A mixed layer nutrientclimatology of leeuwin Current and Western Australian shelfwaters: seasonal nutrient dynamics and biomass. Journal ofMarine Systems 59: 25–51.

McDonald J 2005 Solitary Ascidacea from shallow waters of theArchipelago of the Recherche, Western Australia. In: TheMarine Flora and Fauna of Esperance, Western Australia (edsF E Wells D I Walker & G A Kendrick). Western AustralianMuseum, pp 451–461.

McDonald J & Marsh L 2005 Asteroidea from shallow waters ofthe Recherche Archipelago, Western Australia. In: TheMarine Flora and Fauna of Esperance, Western Australia (edsF E Wells D I Walker & G A Kendrick). Western AustralianMuseum, pp 463–475.

McGowran B, Li Q, Cann J, Padley D, McKirdy D M & Shafik S1997 Biogeographic impact of the Leeuwin Current insouthern Australia since the late middle Eocene.Palaeoceanography, Palaeoclimatology, Palaeoecology 136:1940.

Murray-Wallace C V, Geu A G, Kendrick G W, Brown L J,Belperio A P & Sherwood J E 2001 Palaeoclimateimplications of the occurrence of the arcoid bivalve Andaratrapezia (Deshayes) in the Quarternary of Australasia.Quarternary Science Reviews 19: 559–590.

O’Hara T D 2001 Consistency of faunal and floral assemblageswithin temperate subtidal rocky reef habitats. Marine &Freshwater Research 52: 853–863.

O’Hara T D & Poore G C B 2000 Distribution and origin ofsouthern Australian echinoderms and decapods. Journal ofBiogeography 27: 1321–1335.

Phillips J A 2001 Marine macroalgal biodiversity hotspots: whyis there high species richness and endemism in southernAustralian marine benthic flora? Biodiversity &Conservation 10: 1555–1577.

Poore G C B 1994 Marine biogeography of Australia. In: MarineBiology (eds L S Hammond & R N Synnot). LongmanCheshire, pp 189–213.

Ryan D A, Brooke B P, Collins L P, Kendrick G A, Baxter K P,Bickers A N, Siwabessy P J W & Pattiaratchi C B 2007 Theinfluence of geomorphology and sedimentary processes onshallow water benthic habitat distribution: Esperance Bay,Western Australia. Estuarine Coastal and Shelf Science 72:379–386.

Toohey B D, Kendrick G A & Harvey E S 2007 Disturbance andreef topography maintain high local diversity in Eckloniaradiata kelp forests Oikos 116: 1618–1630.

Toohey B D & Kendrick G A 2008 Canopy understoreyrelationships are mediated by reef topography in Eckloniaradiata kelp beds. European Journal of Phycology 43: 133–142.

Valdovinos C, Navarrete S A & Marquet P A 2003 Molluskspecies diversity in the southeastern Pacific: why are theremore species towards the pole? Ecography 26: 139–144.

Veevers J J 1991 Phanerozoic Australia in the changingconfiguration of Proto-Pangea through Gondwanaland andPangea to the present dispersed continents. AustralianSystematic Botany 4: 1–11.

von der Borch C C 1968 Southern Australian submarinecanyons: their distribution and ages. Marine Geology 6: 267–279.

Watson J E 2005 Hydroids of the Archipelago of the Rechercheand Esperance, Western Australia: Annotated listredescription of species and description of new species. In:The Marine Flora and Fauna of Esperance, Western Australia(eds F E Wells, D I Walker & G A Kendrick). WesternAustralian Museum, pp 495–611.

Wells F E, Longbottom A F & Longbottom J 2005 The marinemolluscs of Esperance Bay and the Recherche Archipelago,Western Australia. In: The Marine Flora and Fauna ofEsperance, Western Australia (eds F E Wells, D I Walker& G A Kendrick). Western Australian Museum, pp 289–313.

Wells P E & Wells G M 1994 Large scale reorganization of oceancurrents offshoreWestern Australia during the lateQuarternary. Marine Micropalaeotology 24: 157–186.

Wernberg T, Kendrick G A & Phillips J C 2003 Regionaldifferences in kelpassociated algal assemblages on temperatelimestone reefs in southwestern Australia. Diversity &Distributions 9: 427–441.

Williams A, Koslow JA & Last PR 2001 Diversity density andcommunity structure of the demersal fish fauna of thecontinental slope of western Australia (20 to 35°S). MarineEcology Progress Series 212: 247–263..

Womersley H B S 1984 The marine benthic flora of SouthernAustralia Part I. South Australian Government PrintingDivision.

Womersley H B S 1987 The marine benthic flora of SouthernAustralia Part II. South Australian Government PrintingDivision.

Womersley H B S 1990 Biogeography of Australasian marinemacroalgae In: Biology of Marine Plants (eds M N Clayton &R J King). Longman Cheshire Pty Limited, pp 368–381.

Womersley H B S 1994 The marine benthic flora of SouthernAustralia Part IIIA. Australian Biological Resources Study.

Womersley H B S 1996 The marine benthic flora of SouthernAustralia Part IIIB. Australian Biological Resources Study.

Womersley H B S 1998 The marine benthic flora of SouthernAustralia Part IIIC. Australian Biological Resources Study.

Womersley H B S 2003 The marine benthic flora of SouthernAustralia Part IIID. Australian Biological Resources Study.

Womersley H B S & Baldock R N 2003 The Encounter 2002expedition to the Isles of St Francis, South Australia: Marinebenthic algae. Transactions of the Royal Society of SouthAustralia 127: 141–151.


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